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Biogeography and Colonization History of Plethodontid Salamanders From Journal of Biogeography (J. Biogeogr.) (2016) 43, 410–422 ORIGINAL Biogeography and colonization history ARTICLE of plethodontid salamanders from the Interior Highlands of eastern North America Samuel D. Martin1*, Donald B. Shepard2, Michael A. Steffen1, John G. Phillips1 and Ronald M. Bonett1 1Department of Biological Science, University ABSTRACT of Tulsa, 800 S. Tucker Drive, Tulsa, OK Aim The Interior Highlands (Ouachita Mountains and Ozark Plateau) are 74104, USA, 2Department of Biology, major physiographical regions of eastern North America and harbour many University of Central Arkansas, 201 Donaghey Ave., LSC 180, Conway, AR 72035, endemic species. Despite their close proximity, the Ozarks and Ouachitas have USA different geological histories and relatively distinct species pools. Few studies have tested the biogeographical origins of this region’s fauna, and most researchers have treated the Interior Highlands as a single unit. Here, we inferred the sources and timing of colonization of the Ozarks and the Ouachi- tas by analysing the biogeography of three genera of plethodontid salamanders (Eurycea, Plethodon and Desmognathus). Location Eastern North America. Methods We constructed a well-sampled, time-calibrated phylogeny for the family Plethodontidae using three mitochondrial and three nuclear genes in beast. Genetic data were primarily taken from GenBank, although we also pro- duced 76 novel sequences. Using lagrange, we reconstructed ancestral areas for North American plethodontids. We compared the frequency and timing of disper- sal events between the Ozarks and Ouachitas to other putative sources such as the Eastern Highlands (Appalachian Mountains and associated limestone plateaus). Results We inferred nine dispersal events from the Eastern Highlands to the Interior Highlands, and just two dispersal events between the geographically proximate Ozarks and Ouachitas. Following one dispersal in the Oligocene, other inter-highland dispersal events occurred in the Miocene and Pliocene, including two periods of near-synchronous movements. Main conclusions Given the relatively limited faunal exchange between the Ozarks and Ouachitas, we conclude that either the river valley separating the Ozarks and Ouachitas is a more formidable barrier to plethodontid salamander dispersal than barriers separating the Interior Highlands from the Eastern Highlands, or ecological/community contingencies have limited dispersal within the Interior Highlands. In our study, geographical proximity of upland islands does not correspond with faunal similarity. *Correspondence: Samuel D. Martin, Keywords Department of Biological Science, University of Amphibia, ancestral area reconstruction, Appalachian Mountains, comparative Tulsa, 800 S. Tucker Drive, Tulsa, OK 74104, biogeography, dispersal, Mississippi River, Ouachita Mountains, Ozark Pla- USA. E-mail: [email protected] teau, Plethodontidae, sky island (MacArthur & Wilson, 1963, 1967). The ages and connectiv- INTRODUCTION ity of ‘sky island’ habitats (Heald, 1951) have influenced the Dispersal among habitat islands generally becomes more dif- biodiversity of many organisms that are unable to disperse ficult with increasing isolation and decreasing island size across lower elevations (reviewed by McCormack et al., 410 http://wileyonlinelibrary.com/journal/jbi ª 2015 John Wiley & Sons Ltd doi:10.1111/jbi.12625 Dispersal by salamanders among North American highland areas 2009). Therefore, highland regions in geographical proximity and range continuity. However, in recent decades extensive should have more similar faunas (or more frequent gene DNA sequence data sets have been generated for eastern flow), while more distant regions should have less faunal North American plethodontids, as well as methods for diver- exchange. gence time estimation and ancestral area reconstruction The highland regions of eastern North America are major which can be used to better test these hypotheses. centres of endemism and diversity for many mesic-adapted Although the biogeography of eastern North American organisms, including amphibians (Duellman & Sweet, 1999), plethodontids has been analysed (Kozak et al., 2009; Bonett crayfishes (Crandall & Buhay, 2008) and freshwater fishes et al., 2014), previous authors treated the Ozarks and Oua- (Mayden, 1988). This is due to many factors, including their chitas as a single biogeographical unit (Interior Highlands), geological and climatic stability, complex topography and despite their distinct faunas. To date, no study has tested the drainage systems, abundant springs (limestone geology), and unique biogeographical origins of Ozark and Ouachita relatively consistent precipitation (Cross et al., 1986). The lar- plethodontid salamanders. Here, we construct a time-cali- gest highland region in eastern North America is the Eastern brated phylogenetic hypothesis for the family Plethodontidae Highlands, which includes the Appalachian Mountains and to infer the evolution of geographical ranges. From these adjacent uplands. reconstructions, we determine the geographical origins of Across the Mississippi River Valley to the west lie two Ozark and Ouachita plethodontids and compare the fre- smaller highland regions (Ouachita Mountains and Ozark quency of dispersal events among the three highland regions Plateau), referred to collectively as the Interior Highlands. of eastern North America. Lastly, we use divergence time The Ozark Plateau is a dissected limestone uplift, and the estimates to test for asynchrony of reconstructed dispersal Ouachita Mountains are a series of folded mountains, similar events. to the Appalachians but oriented on an east–west axis. Cur- rently separated by the Arkansas River Valley, these adjacent MATERIALS AND METHODS highlands were formed by disparate geological processes, but both date to the Ouachita orogeny during the Pennsylvanian Phylogenetic reconstruction (Thornbury, 1965), and have since weathered extensively. Therefore, these highlands pre-date the origin of plethodon- We sampled most recognized species of North American tid salamanders by at least 200 Myr (Mueller, 2006; Zhang & plethodontids, and several divergent lineages that potentially Wake, 2009; Bonett et al., 2014). Despite their geographical represent undescribed species, for a total of 230 terminal proximity (as close as ~38 km), the Ozarks and Ouachitas plethodontid taxa. We included two outgroup taxa, Rhya- have distinct faunas, with over 160 and 48 endemic species cotriton variegatus (Rhyacotritonidae) and Amphiuma respectively (Ouachita Ecoregional Assessment Team, The tridactylum (Amphiumidae; see Appendix S1 in Supporting Nature Conservancy, 2003; Ozarks Ecoregional Assessment Information for species authorities). These represent families Team, The Nature Conservancy, 2003). reconstructed as closely related to plethodontids in recent Few taxonomically broad studies concerning the origins of higher level molecular phylogenies of salamanders (Chippin- Interior Highland taxa have been conducted, although the dale et al., 2004; Wiens et al., 2006; Roelants et al., 2007; fish fauna was the subject of several influential (but primarily Zhang & Wake, 2009; Pyron & Wiens, 2011). We only sam- descriptive) works nearly three decades ago (Mayden, 1985, pled two to three representatives from each of the diverse 1987, 1988; Wiley & Mayden, 1985); Mayden (1985) also Central and South American plethodontid genera (tribe Boli- briefly discussed salamanders and crayfishes. Collectively, toglossini) because these in situ radiations would not impact these authors concluded that the Appalachians, Ozarks and our North American ancestral area reconstructions, and Ouachitas were contiguous until the Pleistocene, when they omitting them increased computational efficiency. We refer- were fragmented by glaciation and associated processes. In enced several published and unpublished intraspecific phylo- contrast, Crandall & Templeton (1999) found evidence for genies to inform our taxon sampling, and included multiple multiple episodes of dispersal and vicariance among highland representatives of species with particular relevance to our regions in the diverse crayfish genus Orconectes. reconstruction, especially species with geographically diver- In one of the first discussions of Interior Highland bio- gent lineages distributed in multiple regions. geography, Dowling (1956) noted that salamanders had the Our alignment included three mitochondrial genes: cyto- most informative distributions for reconstructing past bio- chrome b (Cytb), and NADH dehydrogenase subunits 2 geographical events, due to their strict habitat requirements (ND2) and 4 (ND4); and three nuclear genes: the recombina- and low dispersal abilities. This is especially pronounced in tion activating protein 1 gene (Rag1), pro-opiomelanocortin lungless salamanders of the family Plethodontidae. Dowling (POMC) and brain derived neurotrophic factor (BDNF). concluded that there were four primary colonizing elements, Most of the DNA sequences used were obtained from including what he considered a ‘pre-glacial’ group from the GenBank or other authors (716), but we also generated 74 Appalachians. As a rough metric to estimate timing of diver- novel sequences for this study following methods described gence, Dowling (1956) used taxonomic level (i.e. species ver- previously (Shepard & Burbrink, 2008; Bonett et al., 2014). sus subspecies), morphological and ecological differentiation, Newly generated sequences were deposited on GenBank (see Journal
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